Effects of multiple metal binding sites on calcium and magnesium-dependent activation of BK channels

Journal of General Physiology

Volumn 127, Issue 1, 2006, Pages 35-49

  Hu, Lei ^a   Yang, Huanghe ^a   Shi, Jingyi ^a   Cui, Jianmin ^a  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM ACTIVATED POTASSIUM CHANNEL; MAGNESIUM;

ARTICLE; BINDING AFFINITY; BINDING SITE; DATA ANALYSIS; GENE EXPRESSION; MEMBRANE CONDUCTANCE; MOLECULAR CLONING; MUTAGENESIS; STEADY STATE;

ALLOSTERIC SITE; ANIMALS; BINDING SITES; CALCIUM; FEMALE; ION CHANNEL GATING; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MAGNESIUM; MATHEMATICS; MEMBRANE POTENTIALS; MODELS, BIOLOGICAL; MUTATION; OOCYTES; XENOPUS LAEVIS;

EID: 29844446588     PISSN: 00221295     EISSN: 00221295     Source Type: Journal    
DOI: 10.1085/jgp.200509317     Document Type: Article

References (98)

1. + current in vertebrate sympathetic neurones. Nature. 296:746-749.
2. Adelman, J.P., K.Z. Shen, M.P. Kavanaugh, R.A. Warren, Y.N. Wu, A. Lagrutta, C.T. Bond, and R.A. North. 1992. Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron. 9:209-216.
3. + channel is essential for innate immunity. Nature. 427:853-858.
4. Atkinson, N.S., G.A. Robertson, and B. Ganetzky. 1991. A component of calcium-activated potassium channels encoded by the Drosophila slo locus. Science. 253:551-555.
5. 2+ sensing. J. Gen. Physiol. 123:475-489.
6. 2+ sensitivity. J. Gen. Physiol. 120:173-189.
7. Behrens, R., A. Nolting, F. Reimann, M. Schwarz, R. Waldschutz, and O. Pongs. 2000. hKCNMB3 and hKCNMB4, cloning and characterization of two members of the large-conductance calcium-activated potassium channel β subunit family. FEBS Lett. 474:99-106.
8. Berridge, M.J., P. Lipp, and M.D. Bootman. 2000. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1:11-21.
9. 2+-dependent activation. Proc. Natl. Acad. Sci. USA. 98:4776-4781.
10. + channel. J. Physiol. 533:681-695.
11. Brenner, R., T.J. Jegla, A. Wickenden, Y. Liu, and R.W. Aldrich. 2000a. Cloning and functional characterization of novel large conductance calcium-activated potassium channel β subunits, hKCNMB3 and hKCNMB4. J. Biol. Chem. 275:6453-6461.
12. Brenner, R., G.J. Perez, A.D. Bonev, D.M. Eckman, J.C. Kosek, S.W. Wiler, A.J. Patterson, M.T. Nelson, and R.W. Aldrich. 2000b. Vasoregulation by the β1 subunit of the calcium-activated potassium channel. Nature. 407:870-876.
13. Butler, A., S. Tsunoda, D.P. McCobb, A. Wei, and L. Salkoff. 1993. mSlo, a complex mouse gene encoding "maxi" calcium-activated potassium channels. Science. 261:221-224.
14. Chandler, W.K., and H. Meves. 1965. Voltage clamp experiments on internally perfused giant axons. J. Physiol. 180:788-820.
15. Corkey, B.E., J. Duszynski, T.L. Rich, B. Matschinsky, and J.R. Williamson. 1986. Regulation of free and bound magnesium in rat hepatocytes and isolated mitochondria. J. Biol. Chem. 261:2567-2574.
16. 2+ sensitivity. J. Gen. Physiol. 116:411-432.
17. + channel. J. Gen. Physiol. 110:257-281.
18. + channels. J. Gen. Physiol. 109:633-646.
19. + channels. Biochemistry. 39:15612-15619.
20. + channels. J. Gen. Physiol. 109:647-673.
21. Delva, P. 2003a. Magnesium and cardiac arrhythmias. Mol. Aspects Med. 24:53-62.
22. Delva, P. 2003b. Magnesium and coronary heart disease. Mol. Aspects Med. 24:63-78.
23. Delva, P. 2003c. Magnesium and heart failure. Mol. Aspects Med. 24:79-105.
24. Dworetzky, S.I., J.T. Trojnacki, and V.K. Gribkoff. 1994. Cloning and expression of a human large-conductance calcium-activated potassium channel. Brain Res. Mol. Brain Res. 27:189-193.
25. Fabiato, A., and F. Fabiato. 1979. Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J. Physiol. (Paris). 75:463-505.
26. 2+ also block. J. Gen. Physiol. 98:163-181.
27. Fettiplace, R., and P.A. Fuchs. 1999. Mechanisms of hair cell tuning. Annu. Rev. Physiol. 61:809-834.
28. Flatman, P.W. 1984. Magnesium transport across cell membranes. J. Membr. Biol. 80:1-14.
29. Flatman, P.W. 1991. Mechanisms of magnesium transport. Annu. Rev. Physiol. 53:259-271.
30. + channels from mammalian skeletal muscle. J. Exp. Biol. 124:5-13.
31. Grahame, D.C. 1947. The electrical double layer and the theory of electrocapillarity. Chem. Rev. 41:441-501.
32. Gupta, R.K., P. Gupta, and R.D. Moore. 1984. NMR studies of intracellular metal ions in intact cells and tissues. Annu. Rev. Biophys. Bioeng. 13:221-246.
33. Hille, B., A.M. Woodhull, and B.I. Shapiro. 1975. Negative surface charge near sodium channels of nerve: divalent ions, monovalent ions, and pH. Philos. Trans. R. Soc. Lond. B Biol. Sci. 270:301-318.
34. 2+ increases the coupling of voltage-sensor activation to channel opening to BK potassium channels. Biophys. J. 88:100A.
35. 2+ binding and channel opening in large conductance (BK) potassium channels. J. Gen. Physiol. 120:267-305.
36. Hudspeth, A.J., and R.S. Lewis. 1988a. Kinetic analysis of voltage-and ion-dependent conductances in saccular hair cells of the bull-frog, Rana catesbeiana. J. Physiol. 400:237-274.
37. Hudspeth, A.J., and R.S. Lewis. 1988b. A model for electrical resonance and frequency tuning in saccular hair cells of the bullfrog, Rana catesbeiana. J. Physiol. 400:275-297.
38. Jiang, Y., A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon. 2002. Crystal structure and mechanism of a calcium-gated potassium channel. Nature. 417:515-522.
39. + channel and demonstration of its presence in the human BK channel. Neuron. 29:593-601.
40. Jiang, Z., M. Wallner, P. Meera, and L. Toro. 1999. Human and rodent MaxiK channel β-subunit genes: cloning and characterization. Genomics. 55:57-67.
41. Ca channels in the muscarinic and β-adrenergic regulation of airway smooth muscle. Am. J. Physiol. 268:L221-L229.
42. Lancaster, B., and R.A. Nicoll. 1987. Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones. J. Physiol. 389:187-203.
43. Laurant, P., and R.M. Touyz. 2000. Physiological and pathophysiological role of magnesium in the cardiovascular system: implications in hypertension. J. Hypertens. 18:1177-1191.
44. + channel from Chara australis. J. Gen. Physiol. 100:269-300.
45. + channel. Biochemistry. 28:8092-8099.
46. 2+channels in hippocampal neurons. Nature. 395:900-905.
47. Marty, A. 1981. Ca-dependent K channels with large unitary conductance in chromaffin cell membranes. Nature. 291:497-500.
48. McLaughlin, S. 1977. Electrostatic potentials at membrane-solution interfaces. Curr. Top. Membr. Transp. 9:71-144.
49. McManus, O.B., L.M. Helms, L. Pallanck, B. Ganetzky, R. Swanson, and R.J. Leonard. 1995. Functional role of the β subunit of high conductance calcium-activated potassium channels. Neuron. 14:645-650.
50. + channels in rat skeletal muscle. J. Physiol. 443:739-777.
51. Meera, P., M. Wallner, Z. Jiang, and L. Toro. 1996. A calcium switch for the functional coupling between α (hslo) and β subunits (KV,Ca β) of maxi K channels. FEBS Lett. 382:84-88.
52. + channel resistant to charybdotoxin and iberiotoxin. Proc. Natl. Acad. Sci. USA. 97:5562-5567.
53. Moss, G.W., J. Marshall, and E. Moczydlowski. 1996a. Hypothesis for a serine proteinase-like domain at the COOH terminus of Slowpoke calcium-activated potassium channels. J. Gen. Physiol. 108:473-484.
54. Moss, G.W., J. Marshall, M. Morabito, J.R. Howe, and E. Moczydlowski. 1996b. An evolutionarily conserved binding site for serine proteinase inhibitors in large conductance calcium-activated potassium channels. Biochemistry. 35:16024-16035.
55. Nelson, M.T., H. Cheng, M. Rubart, L.F. Santana, A.D. Bonev, H.J. Knot, and W.J. Lederer. 1995. Relaxation of arterial smooth muscle by calcium sparks. Science. 270:633-637 (see comments).
56. 2+-activated potassium channels by retaining the gating in the bursting states. J. Gen. Physiol. 113:425-440.
57. + channel from skeletal muscle membrane. J. Gen. Physiol. 92:67-86.
58. Orio, P., and R. Latorre. 2005. Differential Effects of β1 and β2 subunits on BK channel activity. J. Gen. Physiol. 125:395-411.
59. Pallanck, L., and B. Ganetzky. 1994. Cloning and characterization of human and mouse homologs of the Drosophila calcium-activated potassium channel gene, slowpoke. Hum. Mol. Genet. 3:1239-1243.
60. + currents in rat muscle cell culture. Nature. 293:471-474.
61. Perez, G., and L. Toro. 1994. Differential modulation of large-conductance conductance KCa channels by PKA in pregnant and nonpregnant myometrium. Am. J. Physiol. 266:C1459-C1463.
62. Perez, G.J., A.D. Bonev, J.B. Patlak, and M.T. Nelson. 1999. Functional coupling of ryanodine receptors to KCa channels in smooth muscle cells from rat cerebral arteries. J. Gen. Physiol. 113:229-238.
63. Petersen, O.H., and Y. Maruyama. 1984. Calcium-activated potassium channels and their role in secretion. Nature. 307:693-696.
64. Ca potassium channels lacking the calcium bowl and RCK domains. Nature. 420:499-502.
65. 2+ spark/STOC coupling and elevated blood pressure. Circ. Res. 87:E53-E60.
66. 2+, activating mechanisms. Proc. Natl. Acad. Sci. USA. 100:10061-10066.
67. Raffaelli, G., C. Saviane, M.H. Mohajerani, P. Pedarzani, and E. Cherubini. 2004. BK potassium channels control transmitter release at CA3-CA3 synapses in the rat hippocampus. J. Physiol. 557: 147-157.
68. Riazi, M.A., P. Brinkman-Mills, A. Johnson, S.L. Naylor, S. Minoshima, N. Shimizu, A. Baldini, and H.E. McDermid. 1999. Identification of a putative regulatory subunit of a calcium-activated potassium channel in the dup(3q) syndrome region and a related sequence on 22q11.2. Genomics. 62:90-94.
69. Ricci, A.J., M. Gray-Keller, and R. Fettiplace. 2000. Tonotopic variations of calcium signalling in turtle auditory hair cells. J. Physiol. 524(Pt 2):423-436.
70. Roberts, W.M. 1994. Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells. J. Neurosci. 14:3246-3262.
71. Roberts, W.M., R.A. Jacobs, and A.J. Hudspeth. 1990. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J. Neurosci. 10:3664-3684.
72. Robitaille, R., and M.P. Charlton. 1992. Presynaptic calcium signals and transmitter release are modulated by calcium-activated potassium channels. J. Neurosci. 12:297-305.
73. Robitaille, R., M.L. Garcia, G.J. Kaczorowski, and M.P. Charlton. 1993. Functional colocalization of calcium and calcium-gated potassium channels in control of transmitter release. Neuron. 11: 645-655.
74. + (BK) channels in chick hair cells are clustered and colocalized with apical-basal and tonotopic gradients. J. Physiol. 560:13-20.
75. Schreiber, M., and L. Salkoff. 1997. A novel calcium-sensing domain in the BK channel. Biophys. J. 73:1355-1363.
76. Schreiber, M., A. Yuan, and L. Salkoff. 1999. Transplantable sites confer calcium sensitivity to BK channels. Nat. Neurosci. 2:416-421.
77. Seelig, M.S. 2000. Interrelationship of magnesium and congestive heart failure. Wien. Med. Wochenschr. 150:335-341.
78. + channels. J. Gen. Physiol. 118:589-606.
79. Shi, J., G. Krishnamoorthy, Y. Yang, L. Hu, N. Chaturvedi, D. Harilal, J. Qin, and J. Cui. 2002. Mechanism of magnesium activation of calcium-activated potassium channels. Nature. 418:876-880.
80. Storm, J.F. 1987. Action potential repolarization and a fast afterhyperpolarization in rat hippocampal pyramidal cells. J. Physiol. 385:733-759
81. Stretton, D., M. Miura, M.G. Belvisi, and P.J. Barnes. 1992. Calcium-activated potassium channels mediate prejunctional inhibition of peripheral sensory nerves. Proc. Natl. Acad. Sci. USA. 89:1325-1329.
82. Sun, X.P., B. Yazejian, and A.D. Grinnell. 2004. Electrophysiological properties of BK channels in Xenopus motor nerve terminals. J. Physiol. 557:207-228.
83. Tanaka, Y., P. Meera, M. Song, H.G. Knaus, and L. Toro. 1997. Molecular constituents of maxi KCa channels in human coronary smooth muscle: predominant α + β subunit complexes. J. Physiol. 502:545-557.
84. Touyz, R.M. 2003. Role of magnesium in the pathogenesis of hypertension. Mol. Aspects Med. 24:107-136.
85. + channel isoforms from human brain. Neuron. 13:1315-1330.
86. + channel β-subunit from human brain. Proc. Natl. Acad. Sci. USA. 93:9200-9205.
87. Vink, R., and I. Cernak. 2000. Regulation of intracellular free magnesium in central nervous system injury. Front. Biosci. 5:D656-D665.
88. + channels: a transmembrane β-subunit homolog. Proc. Natl. Acad. Sci. USA. 96: 4137-4142.
89. + channels participate in the regulation of pituitary prolactin secretion. Brain Res. 662:83-87.
90. Weiger, T.M., M.H. Holmqvist, I.B. Levitan, F.T. Clark, S. Sprague, W.J. Huang, P. Ge, C. Wang, D. Lawson, M.E. Jurman, et al. 2000. A novel nervous system β subunit that downregulates human large conductance calcium-dependent potassium channels. J. Neurosci. 20:3563-3570.
91. 2+-sensitive ion channels. Cell Calcium. 34:211-229.
92. Wu, Y.C., J.J. Art, M.B. Goodman, and R. Fettiplace. 1995. A kinetic description of the calcium-activated potassium channel and its application to electrical tuning of hair cells. Prog. Biophys. Mol. Biol. 63:131-158.
93. Xia, X.M., X. Zeng, and C.J. Lingle. 2002. Multiple regulatory sites in large-conductance calcium-activated potassium channels. Nature. 418:880-884.
94. Xia, X.M., X. Zhang, and C.J. Lingle. 2004. Ligand-dependent activation of Slo family channels is defined by interchangeable cytosolic domains. J. Neurosci. 24:5585-5591.
95. Yazejian, B., D.A. DiGregorio, J.L. Vergara, R.E. Poage, S.D. Meriney, and A.D. Grinnell. 1997. Direct measurements of presynaptic calcium and calcium-activated potassium currents regulating neurotransmitter release at cultured Xenopus nerve-muscle synapses. J. Neurosci. 17:2990-3001.
96. + channels. Nat. Neurosci. 3:566-571.
97. Zeng, X.H., X.M. Xia, and C.J. Lingle. 2005. Divalent cation sensitivity of BK channel activation supports the existence of three distinct binding sites. J. Gen. Physiol. 125:273-286.
98. 2+ through a nonselective, low affinity divalent cation site. J. Gen. Physiol. 118:607-636.